Antimutator role of DNA glycosylase MutY in pathogenic Neisseria species

Journal of Bacteriology

Volumn 187, Issue 8, 2005, Pages 2801-2809

  Davidsen, T ^a   Bjoras M ^a,b   Seeberg, E C ^a   Tonjum T ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 8 OXO 2' DEOXYGUANOSINE; DNA; DNA GLYCOSYLASE MUTY; RIFAMPICIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; EXCISION REPAIR; GENE EXPRESSION; GENE MUTATION; GENE TRANSFER; IN VIVO STUDY; MENINGOCOCCOSIS; NEISSERIA MENINGITIDIS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RPOB GENE; STRESS; WILD TYPE;

BASE PAIR MISMATCH; DNA GLYCOSYLASES; DNA MUTATIONAL ANALYSIS; DNA REPAIR; GUANINE; NEISSERIA; RECOMBINANT FUSION PROTEINS;

ESCHERICHIA COLI; NEISSERIA; NEISSERIA MENINGITIDIS;

EID: 16844383753     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.8.2801-2809.2005     Document Type: Article

References (53)

1. Bjelland, S., and E. Seeberg. 1987. Purification and characterization of 3-methyladenine DNA glycosylase I from Escherichia coli. Nucleic Acids Res. 15:2787-2801.
2. Boiteux, S., J. Belleney, B. P. Roques, and J. Laval. 1984. Two rotameric forms of open ring 7-methylguanine are present in alkylated polynucleotides. Nucleic Acids Res. 12:5429-5439.
3. Boiteux, S., T. R. O'Connor, F. Lederer, A. Gouyette, and J. Laval. 1990. Homogeneous Escherichia coli FPG protein. A DNA glycosylase which excises imidazole ring-opened purines and nicks DNA at apurinic/apyrimidinic sites. J. Biol. Chem. 265:3916-3922.
4. Bucci, C., A. Lavitola, P. Salvatore, L. Del Giudice, D. R. Massardo, C. B. Bruni, and P. Alifano. 1999. Hypermutation in pathogenic bacteria: frequent phase variation in meningococci is a phenotypic trait of a specialized mutator biotype. Mol. Cell 3:435-445.
5. Cohen, M. S., J. G. Cannon, A. E. Jerse, L. M. Charniga, S. F. Isbey, and L. G. Whicker. 1994. Human experimentation with Neisseria gonorrhoeae: rationale, methods, and implications for the biology of infection and vaccine development. J. Infect. Dis. 169:532-537.
6. Davidsen, T., E. A. Rodland, K. Lagesen, E. Seeberg, T. Rognes, and T. Tonjum. 2004. Biased distribution of DNA uptake sequences towards genome maintenance genes. Nucleic Acids Res. 32:1050-1058.
7. Demple, B., and M. S. DeMott. 2002. Dynamics and diversions in base excision DNA repair of oxidized abasic lesions. Oncogene 21:8926-8934.
8. Demple, B., and L. Harrison. 1994. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63:915-948.
9. Denver, D. R., S. L. Swenson, and M. Lynch. 2003. An evolutionary analysis of the helix-hairpin-helix superfamily of DNA repair glycosylases. Mol. Biol. Evol. 20:1603-1611.
10. de Weert, S., L. C. Dekkers, I. Kuiper, G. V. Bloemberg, and B. J. Lugtenberg. 2004. Generation of enhanced competitive root-tip-colonizing Pseudomonas bacteria through accelerated evolution. J. Bacteriol. 186:3153-3159.
11. Eide, L., M. Bjoras, M. Pirovano, I. Alseth, K. G. Berdal, and E. Seeberg. 1996. Base excision of oxidative purine and pyrimidine DNA damage in Saccharomyces cerevisiae by a DNA glycosylase with sequence similarity to endonuclease III from Escherichia coli. Proc. Natl. Acad. Sci. USA 93:10735-10740.
12. Eisen, J. A., and P. C. Hanawalt. 1999. A phylogenomic study of DNA repair genes, proteins, and processes. Mutat. Res. 435:171-213.
13. Fowler, R. G., S. J. White, C. Koyama, S. C. Moore, R. L. Dunn, and R. M. Schaaper. 2003. Interactions among the Escherichia coli mutT, mutM, and mutY damage prevention pathways. DNA Repair (Amsterdam) 2:159-173.
14. Frasch, C. E., and S. S. Chapman. 1972. Classification of Neisseria meningitidis group B into distinct serotypes. I. Serological typing by a microbactericidal method. Infect. Immun. 5:98-102.
15. Fromme, J. C., A. Banerjee, S. J. Huang, and G. L. Verdine. 2004. Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature 427:652-656.
16. Gifford, C. M., J. O. Blaisdell, and S. S. Wallace. 2000. Multiprobe RNase protection assay analysis of mRNA levels for the Escherichia coli oxidative DNA glycosylase genes under conditions of oxidative stress. J. Bacteriol. 182:5416-5424.
17. Giraud, A., M. Radman, I. Matic, and F. Taddei. 2001. The rise and fall of mutator bacteria. Curr. Opin. Microbiol. 4:582-585.
18. Gu, Y., A. Parker, T. M. Wilson, H. Bai, D. Y. Chang, and A. L. Lu. 2002. Human MutY homolog, a DNA glycosylase involved in base excision repair, physically and functionally interacts with mismatch repair proteins human MutS homolog 2/human MutS homolog 6. J. Biol. Chem. 277:11135-11142.
19. Guan, Y., R. C. Manuel, A. S. Arvai, S. S. Parikh, C. D. Mol, J. H. Miller, S. Lloyd, and J. A. Tainer. 1998. MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat. Struct. Biol. 5:1058-1064.
20. Holten, E. 1979. Serotypes of Neisseria meningitidis isolated from patients in Norway during the first six months of 1978. J. Clin. Microbiol. 9:186-188.
21. Jolley, K. A., L. Sun, E. R. Moxon, and M. C. Maiden. 2004. Dam inactivation in Neisseria meningitidis: prevalence among diverse hyperinvasive lineages. BMC Microbiol. 4:34.
22. Kim, M., T. Huang, and J. H. Miller. 2003. Competition between MutY and mismatch repair at A · C mispairs in vivo. J. Bacteriol. 185:4626-4629.
23. Li, X., and A. L. Lu. 2001. Molecular cloning and functional analysis of the MutY homolog of Deinococcus radiodurans. J. Bacteriol. 183:6151-6158.
24. Lu, A. L., and W. P. Fawcett. 1998. Characterization of the recombinant MutY homolog, an adenine DNA glycosylase, from yeast Schizosaccharomyces pombe. J. Biol. Chem. 273:25098-25105.
25. Lu, A. L., J. J. Tsai-Wu, and J. Cillo. 1995. DNA determinants and substrate specificities of Escherichia coli MutY. J. Biol. Chem. 270:23582-23588.
26. Lu, T., Y. Pan, S. Y. Kao, C. Li, I. Kohane, J. Chan, and B. A. Yankner. 2004. Gene regulation and DNA damage in the ageing human brain. Nature 429:883-891.
27. Maki, H., and M. Sekiguchi. 1992. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355:273-275.
28. McGoldrick, J. P., Y. C. Yeh, M. Solomon, J. M. Essigmann, and A. L. Lu. 1995. Characterization of a mammalian homolog of the Escherichia coli MutY mismatch repair protein. Mol. Cell. Biol. 15:989-996.
29. Meyers, L. A., B. R. Levin, A. R. Richardson, and I. Stojiljkovic. 2003. Epidemiology, hypermutation, within-host evolution and the virulence of Neisseria meningitidis. Proc. R. Soc. Lond. B 270:1667-1677.
30. Michaels, M. L., C. Cruz, A. P. Grollman, and J. H. Miller. 1992. Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc. Natl. Acad. Sci. USA 89:7022-7025.
31. Michaels, M. L., and J. H. Miller. 1992. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J. Bacteriol. 174:6321-6325.
32. Nghiem, Y., M. Cabrera, C. G. Cupples, and J. H. Miller. 1988. The mutY gene: a mutator locus in Escherichia coli that generates G · C→T · A transversions. Proc. Natl. Acad. Sci. USA 85:2709-2713.
33. Nolte, O., M. Muller, S. Reitz, S. Ledig, I. Ehrhard, and H. G. Sonntag. 2003. Description of new mutations in the rpoB gene in rifampicin-resistant Neisseria meningitidis selected in vitro in a stepwise manner. J. Med. Microbiol. 52:1077-1081.
34. O'Connor, T. R., and J. Laval. 1989. Physical association of the 2,6-diamino-4-hydroxy-5N-formamidopyrimidine-DNA glycosylase of Escherichia coli and an activity nicking DNA at apurinic/apyrimidinic sites. Proc. Natl. Acad. Sci. USA 86:5222-5226.
35. Oliver, A., R. Canton, P. Campo, F. Baquero, and J. Blazquez. 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251-1254.
36. O'Rourke, E. J., C. Chevalier, A. V. Pinto, J. M. Thiberge, L. Ielpi, A. Labigne, and J. P. Radicella. 2003. Pathogen DNA as target for host-generated oxidative stress: role for repair of bacterial DNA damage in Helicobacter pylori colonization. Proc. Natl. Acad. Sci. USA 100:2789-2794.
37. Parkhill, J., M. Achtman, K. D. James, S. D. Bentley, C. Churcher, S. R. Klee, G. Morelli, D. Basham, D. Brown, T. Chillingworth, R. M. Davies, P. Davis, K. Devlin, T. Feltwell, N. Hamlin, S. Holroyd, K. Jagels, S. Leather, S. Moule, K. Mungall, M. A. Quail, M. A. Rajandream, K. M. Rutherford, M. Simmonds, J. Skelton, S. Whitehead, B. G. Spratt, and B. G. Barrell. 2000. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404:502-506.
38. Reese, M. G. 2001. Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput. Chem. 26:51-56.
39. Riazuddin, S., and T. Lindahl. 1978. Properties of 3-methyladenine-DNA glycosylase from Escherichia coli. Biochemistry 17:2110-2118.
40. Richardson, A. R., and I. Stojiljkovic. 2001. Mismatch repair and the regulation of phase variation in Neisseria meningitidis. Mol. Microbiol. 40:645-655.
41. Richardson, A. R., Z. Yu, T. Popovic, and I. Stojiljkovic. 2002. Mutator clones of Neisseria meningitidis in epidemic serogroup A disease. Proc. Natl. Acad. Sci. USA 99:6103-6107.
42. Sampson, J. R., S. Dolwani, S. Jones, D. Eccles, A. Ellis, D. G. Evans, I. Frayling, S. Jordan, E. R. Maher, T. Mak, J. Maynard, F. Pigatto, J. Shaw, and J. P. Cheadle. 2003. Autosomal recessive colorectal adenomatous polyposis due to inherited mutations of MYH. Lancet 362:39-41.
43. Samrakandi, M. M., and F. Pasta. 2000. Hyperrecombination in Streptococcus pneumonias depends on an atypical mutY homologue. J. Bacteriol. 182:3353-3360.
44. Seeberg, E. 1978. Reconstitution of an Escherichia coli repair endonuclease activity from the separated uvrA+ and uvrB+/uvrC+ gene products. Proc. Natl. Acad. Sci. USA 75:2569-2573.
45. Seeberg, E., L. Eide, and M. Bjoras. 1995. The base excision repair pathway. Trends Biochem. Sci. 20:391-397.
46. Shao, X., and N. V. Grishin. 2000. Common fold in helix-hairpin-helix proteins. Nucleic Acids Res. 28:2643-2650.
47. Stein, D. C., R. J. Danaher, and T. M. Cook. 1991. Characterization of a gyrB mutation responsible for low-level nalidixic acid resistance in Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 35:622-626.
48. Tchou, J., H. Kasai, S. Shibutani, M. H. Chung, J. Laval, A. P. Grollman, and S. Nishimura. 1991. 8-oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity. Proc. Natl. Acad. Sci. USA 88:4690-4694.
49. Tettelin, H., N. J. Saunders, J. Heidelberg, A. C. Jeffries, K. E. Nelson, J. A. Eisen, K. A. Ketchum, D. W. Hood, J. F. Peden, R. J. Dodson, W. C. Nelson, M. L. Gwinn, R. DeBoy, J. D. Peterson, E. K. Mickey, D. H. Haft, S. L. Salzberg, O. White, R. D. Fleischmann, B. A. Dougherty, T. Mason, A. Ciecko, D. S. Parksey, E. Blair, H. Cittone, E. B. Clark, M. D. Cotton, T. R. Utterback, H. Khouri, H. Qin, J. Vamathevan, J. Gill, V. Scarlato, V. Masignani, M. Pizza, G. Grandi, L. Sun, H. O. Smith, C. M. Fraser, E. R. Moxon, R. Rappuoli, and J. C. Venter. 2000. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287:1809-1815.
50. Tonjum, T., N. E. Freitag, E. Namork, and M. Koomey. 1995. Identification and characterization of pilG, a highly conserved pilus-assembly gene in pathogenic Neisseria. Mol. Microbiol. 16:451-464.
51. Tsai-Wu, J.-J., H.-F. Liu, and A.-L. Lu. 1992. Escherichia coli MutY protein has both N-glycosylase and apurinic/apyrimidinic endonuclease activities on A · C and A · G mispairs. Proc. Natl. Acad. Sci. USA 89:8779-8783.
52. Yamada, M., M. S. Kabir, and R. Tsunedomi. 2003. Divergent promoter organization may be a preferred structure for gene control in Escherichia coli. J. Mol. Microbiol. Biotechnol. 6:205-210.
53. Zhao, J., and M. E. Winkler. 2000. Reduction of GC→TA transversion mutation by overexpression of MutS in Escherichia coli K-12. J. Bacteriol. 182:5025-5028.